A male-specific role for SOX9 in vertebrate sex determination

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JOURNAL ARTICLES

A male-specific role for SOX9 in vertebrate sex determination

J Kent, SC Wheatley, JE Andrews, AH Sinclair and P Koopman
Centre for Molecular and Cellular Biology, The University of Queensland, Brisbane, Australia.

Mutation analyses of patients with campomelic dysplasia, a bone dysmorphology and XY sex reversal syndrome, indicate that the SRY-related gene SOX9 is involved in both skeletal development and sex determination. To clarify the role SOX9 plays in vertebrate sex determination, we have investigated its expression during gonad development in mouse and chicken embryos. In the mouse, high levels of Sox9 mRNA were found in male (XY) but not female (XX) genital ridges, and were localised to the sex cords of the developing testis. Purified fetal germ cells lacked Sox9 expression, indicating that Sox9 expression is specific to the Sertoli cell lineage. Sex specificity of SOX9 protein expression was confirmed using a polyclonal antiserum. The timing and cell-type specificity of Sox9 expression suggests that Sox9 may be directly regulated by SRY. Male-specific expression of cSOX9 mRNA during the sex determination period was also observed in chicken genital ridges. The conservation of sexually dimorphic expression in two vertebrate classes which have significant differences in their sex determination mechanisms, points to a fundamental role for SOX9 in testis determination in vertebrates. Sox9 expression was maintained in the mouse testis during fetal and adult life, but no expression was seen at any stage by in situ hybridisation in the developing ovary. Male-specific expression was also observed in the cells surrounding the Mullerian ducts and in the epididymis, and expression in both sexes was detected in the developing collecting ducts of the metanephric kidney. These results suggest that SOX9 may have a wider role in the development of the genitourinary system.

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				S. Ijiri, H. Kaneko, T. Kobayashi, D.-S. Wang, F. Sakai, B. Paul-Prasanth, M. Nakamura, and Y. Nagahama Sexual Dimorphic Expression of Genes in Gonads During Early Differentiation of a Teleost Fish, the Nile Tilapia Oreochromis niloticus Biol Reprod, February 1, 2008; 78(2): 333 - 341. [Abstract] [Full Text] [PDF]

				Y. Kim, N. Bingham, R. Sekido, K. L. Parker, R. Lovell-Badge, and B. Capel Fibroblast growth factor receptor 2 regulates proliferation and Sertoli differentiation during male sex determination PNAS, October 16, 2007; 104(42): 16558 - 16563. [Abstract] [Full Text] [PDF]

				P. Val, J.-P. Martinez-Barbera, and A. Swain Adrenal development is initiated by Cited2 and Wt1 through modulation of Sf-1 dosage Development, June 15, 2007; 134(12): 2349 - 2358. [Abstract] [Full Text] [PDF]

				E. Sumi, N. Iehara, H. Akiyama, T. Matsubara, A. Mima, H. Kanamori, A. Fukatsu, D. J. Salant, T. Kita, H. Arai, et al. SRY-Related HMG Box 9 Regulates the Expression of Col4a2 through Transactivating Its Enhancer Element in Mesangial Cells Am. J. Pathol., June 1, 2007; 170(6): 1854 - 1864. [Abstract] [Full Text] [PDF]

				T. Svingen, A. Beverdam, P. Bernard, P. McClive, V. R Harley, A. H Sinclair, and P. Koopman Sex-specific expression of a novel gene Tmem184a during mouse testis differentiation Reproduction, May 1, 2007; 133(5): 983 - 989. [Abstract] [Full Text] [PDF]

				D. Wilhelm, R. Hiramatsu, H. Mizusaki, L. Widjaja, A. N. Combes, Y. Kanai, and P. Koopman SOX9 Regulates Prostaglandin D Synthase Gene Transcription in Vivo to Ensure Testis Development J. Biol. Chem., April 6, 2007; 282(14): 10553 - 10560. [Abstract] [Full Text] [PDF]

				F. Gao, S. Maiti, N. Alam, Z. Zhang, J. M. Deng, R. R. Behringer, C. Lecureuil, F. Guillou, and V. Huff The Wilms tumor gene, Wt1, is required for Sox9 expression and maintenance of tubular architecture in the developing testis PNAS, August 8, 2006; 103(32): 11987 - 11992. [Abstract] [Full Text] [PDF]

				S. Rajender, V. Rajani, N. J. Gupta, B. Chakravarty, L. Singh, and K. Thangaraj SRY-negative 46,XX male with normal genitals, complete masculinization and infertility Mol. Hum. Reprod., May 1, 2006; 12(5): 341 - 346. [Abstract] [Full Text] [PDF]

				A. Beverdam and P. Koopman Expression profiling of purified mouse gonadal somatic cells during the critical time window of sex determination reveals novel candidate genes for human sexual dysgenesis syndromes Hum. Mol. Genet., February 1, 2006; 15(3): 417 - 431. [Abstract] [Full Text] [PDF]

				F. Barrionuevo, S. Bagheri-Fam, J. Klattig, R. Kist, M. M. Taketo, C. Englert, and G. Scherer Homozygous Inactivation of Sox9 Causes Complete XY Sex Reversal in Mice Biol Reprod, January 1, 2006; 74(1): 195 - 201. [Abstract] [Full Text] [PDF]

				X. Huang, Y. Guo, Y. Shui, S. Gao, H. Yu, H. Cheng, and R. Zhou Multiple Alternative Splicing and Differential Expression of dmrt1 During Gonad Transformation of the Rice Field Eel Biol Reprod, November 1, 2005; 73(5): 1017 - 1024. [Abstract] [Full Text] [PDF]

				A. Jeanes, D. Wilhelm, M. J Wilson, J. Bowles, P. J McClive, A. H Sinclair, and P. Koopman Evaluation of candidate markers for the peritubular myoid cell lineage in the developing mouse testis Reproduction, October 1, 2005; 130(4): 509 - 516. [Abstract] [Full Text] [PDF]

				Y. Kanai, R. Hiramatsu, S. Matoba, and T. Kidokoro From SRY to SOX9: Mammalian Testis Differentiation J. Biochem., July 1, 2005; 138(1): 13 - 19. [Abstract] [Full Text] [PDF]

				C. J. Guigon, N. Coudouel, S. Mazaud-Guittot, M. G. Forest, and S. Magre Follicular Cells Acquire Sertoli Cell Characteristics after Oocyte Loss Endocrinology, July 1, 2005; 146(7): 2992 - 3004. [Abstract] [Full Text] [PDF]

				S. Matoba, Y. Kanai, T. Kidokoro, M. Kanai-Azuma, H. Kawakami, Y. Hayashi, and M. Kurohmaru A novel Sry-downstream cellular event which preserves the readily available energy source of glycogen in mouse sex differentiation J. Cell Sci., April 1, 2005; 118(7): 1449 - 1459. [Abstract] [Full Text] [PDF]

				A. K. Hett, C. Pitra, I. Jenneckens, and A. Ludwig Characterization of Sox9 in European Atlantic Sturgeon (Acipenser sturio) J. Hered., March 1, 2005; 96(2): 150 - 154. [Abstract] [Full Text] [PDF]

				M. J. Wilson, P. Jeyasuria, K. L. Parker, and P. Koopman The Transcription Factors Steroidogenic Factor-1 and SOX9 Regulate Expression of Vanin-1 during Mouse Testis Development J. Biol. Chem., February 18, 2005; 280(7): 5917 - 5923. [Abstract] [Full Text] [PDF]

				C. Poirier, Y. Qin, C. P. Adams, Y. Anaya, J. B. Singer, A. E. Hill, E. S. Lander, J. H. Nadeau, and C. E. Bishop A Complex Interaction of Imprinted and Maternal-Effect Genes Modifies Sex Determination in Odd Sex (Ods) Mice Genetics, November 1, 2004; 168(3): 1557 - 1562. [Abstract] [Full Text] [PDF]

				J. Schmahl, Y. Kim, J. S. Colvin, D. M. Ornitz, and B. Capel Fgf9 induces proliferation and nuclear localization of FGFR2 in Sertoli precursors during male sex determination Development, August 1, 2004; 131(15): 3627 - 3636. [Abstract] [Full Text] [PDF]

				P. Blache, M. van de Wetering, I. Duluc, C. Domon, P. Berta, J.-N. Freund, H. Clevers, and P. Jay SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes J. Cell Biol., July 5, 2004; 166(1): 37 - 47. [Abstract] [Full Text] [PDF]

				J. E. Shima, D. J. McLean, J. R. McCarrey, and M. D. Griswold The Murine Testicular Transcriptome: Characterizing Gene Expression in the Testis During the Progression of Spermatogenesis Biol Reprod, July 1, 2004; 71(1): 319 - 330. [Abstract] [Full Text] [PDF]

				Y. Qin, L.-k. Kong, C. Poirier, C. Truong, P. A. Overbeek, and C. E. Bishop Long-range activation of Sox9 in Odd Sex (Ods) mice Hum. Mol. Genet., June 15, 2004; 13(12): 1213 - 1218. [Abstract] [Full Text] [PDF]

				M.-C. Chaboissier, A. Kobayashi, V. I. P. Vidal, S. Lutzkendorf, H. J. G. van de Kant, M. Wegner, D. G. de Rooij, R. R. Behringer, and A. Schedl Functional analysis of Sox8 and Sox9 during sex determination in the mouse Development, May 1, 2004; 131(9): 1891 - 1901. [Abstract] [Full Text] [PDF]

				H. Akiyama, M.-C. Chaboissier, R. R. Behringer, D. H. Rowitch, A. Schedl, J. A. Epstein, and B. de Crombrugghe Essential role of Sox9 in the pathway that controls formation of cardiac valves and septa PNAS, April 27, 2004; 101(17): 6502 - 6507. [Abstract] [Full Text] [PDF]

				R Pop, C Conz, K S Lindenberg, S Blesson, B Schmalenberger, S Briault, D Pfeifer, and G Scherer Screening of the 1 Mb SOX9 5' control region by array CGH identifies a large deletion in a case of campomelic dysplasia with XY sex reversal J. Med. Genet., April 1, 2004; 41(4): e47 - e47. [Full Text] [PDF]

				N. Moreno-Mendoza, L. Torres-Maldonado, J. Chimal-Monroy, V. Harley, and H. Merchant-Larios Disturbed Expression of Sox9 in Pre-Sertoli Cells Underlies Sex-Reversal in Mice B6.Ytir Biol Reprod, January 1, 2004; 70(1): 114 - 122. [Abstract] [Full Text] [PDF]

				P. G. Buxton, B. Hall, C. W. Archer, and P. Francis-West Secondary chondrocyte-derived Ihh stimulates proliferation of periosteal cells during chick development Development, October 1, 2003; 130(19): 4729 - 4739. [Abstract] [Full Text] [PDF]